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The Orbitofacial Glands of Bats: An Investigation of the Potential Correlation of Gland Structure with Social Organization
Article first published online: 22 JUL 2010
Copyright © 2010 Wiley-Liss, Inc.
The Anatomical Record
Volume 293, Issue 8, pages 1433–1448, August 2010
How to Cite
Rehorek, S. J., Smith, T. D. and Bhatnagar, K. P. (2010), The Orbitofacial Glands of Bats: An Investigation of the Potential Correlation of Gland Structure with Social Organization. Anat Rec, 293: 1433–1448. doi: 10.1002/ar.21046
- Issue published online: 22 JUL 2010
- Article first published online: 22 JUL 2010
- Manuscript Accepted: 27 AUG 2009
- Manuscript Received: 12 AUG 2009
- caruncular sebaceous gland;
- Harderian gland;
- lacrimal gland;
- Meibomian gland;
- orbitofacial glands;
- social organization
- Top of page
- MATERIALS AND METHODS
- GENERAL DISCUSSION
- LITERATURE CITED
The facial glands of bats are modified skin glands, whereas there are up to three different orbital glands: Harderian, lacrimal, and Meibomian glands. Scattered studies have described the lacrimal and Meibomian glands in a handful of bat species, but there is as yet no description of a Harderian gland in bats. In this study we examined serial sections of orbitofacial glands in eight families of bats. Much variation amongst species was observed, with few phylogenetic patterns emerging. Enlarged facial glands, either sudoriparous (five genera) or sebaceous (vespertilionids only) were observed. Meibomian and lacrimal glands were present in most species examined (except Antrozous), though the relative level of development varied. Two types of anterior orbital glands were distinguished: the Harderian gland (tubulo-acinar: observed in Rousettus, Atribeus, Desmodus and Miniopterus) and caruncular (sebaceous: observed in Eptesicus and Dieamus). The relative development of the nasolacrimal duct and the vomeronasal organ did not appear to be correlated with the development of any of the exocrine glands examined. There does, however, appear to be a correlation between the presence of at least one well developed exocrine gland and the level of communality and known olfactory acuity, best documented in Artibeus, Desmodus, and Miniopterus. Anat Rec 293:1433–1448, 2010. © 2010 Wiley-Liss, Inc.
Very little is known about the cranial exocrine glands of the head in bats. Two main groups of such glands are those in the facial and orbital regions (Fig. 1). Some information is available about the relative development of facial glands in bats (Quay,1970; Kulzer et al.,1985; Haffner,1995,2000), though most of this literature focuses on the glands in the mandibular region (chin, gular, intermandibular: see Caspers et al.,2009), with relatively little attention paid to the glands in the maxillary region. Generally speaking, the facial glands are modified sweat (sudoriparous) or sebaceous glands. There are three exocrine skin gland types, classified by mechanism of secretion and opening of duct. Eccrine (merocrine secretion) sweat glands release their contents onto the surface of the skin. Apocrine sweat and sebaceous (holocrine) glands release their secretions into the hair follicle. These glands together appear to produce a compound which plays a role in chemical communication (scent marking etc.) (see Castaneda et al.,2007 for review).
Considerably less is known about the orbital glands of bats. In other mammals there are typically three main types of large orbital glands present: lacrimal, Meibomian (tarsal) and Harderian. Of these the lacrimal gland is usually found in the outer canthus, though it may be present as a palpebral structure in some tetrapods (Rehorek et al.,2005a). This gland has been examined only in one species of bat, Hipposideros speoris (Korad and Joshi,1992). The Meibomian (or tarsal) glands are commonly found in the eyelids. The nomenclature of these glands appears to be interchangeable, and their association with the tarsus of the eyelid (Gartner and Hiatt,2007) has often led to them being referred to as tarsal glands. There are no known descriptions of the bat Meibominan glands. In general, the secretions of both the lacrimal and Meibomian glands are presumed to be a source of lubrication for the cornea, the former producing tears (functioning to protect and moisten the surface of the cornea and associated areas) and the latter creating an oily layer on the tear film to reduce evaporation rates (Gartner and Hiatt,2007).
The Harderian gland is an anterior orbital gland, often associated with the nictitating membrane. It is present in most terrestrial vertebrates, but the function of this gland remains elusive (see Payne,1994 for review). It has been proposed that the Harderian gland may play a role in the vomeronasal system: this is suggested by the anatomical connection between the Harderian gland and the vomeronasal organ (VNO) via the nasolacrimal duct (NLD) which can be observed in many tetrapods (Hillenius and Rehorek,2005). Harderian gland secretions are known to pass into the VNO, via the NLD in caecilians (Wake,1985), snakes (Rehorek et al.,2000) and may also do so in frogs (Hillenius et al.,2001). In mammals, however, the connections of these three structures are less clear (e.g., Rossie and Smith,2007). Not all mammals possess Harderian glands (Paule,1957; Sakai,1981), although in some, the Harderian gland was only recently discovered. For example, a recent re-examination of primates showed the presence of a Harderian gland across the order (Rehorek and Smith,2006). This raises the question of whether the Harderian glands of bats, like that of primates, may have been overlooked in earlier reports. The sole previous study on bats examined only a few specimens with little or no detailed description of the methodology used. There were only two species of bats (Desmodus rotundus and Myotis lucifugus) examined by Paule (1957) with no Harderian gland observed in either one. In primates, histological examination was necessary before the presence of the Harderian gland was discovered (Rehorek and Smith,2006). Consequently, careful histological examination is needed before the presence or absence of this gland in bats is deduced. Considerably more is known about the NLD (Göbbel,2002) and the VNO (Cooper and Bhatnagar,1976; Wible and Bhatnagar,1996) of bats.
The purpose of this study was to examine the relative development of facial and orbital glands in a wide phylogenetic survey of bats. Bats, which may exceed 1,100 species (Locke,2008), are highly diverse especially in terms of facial morphology (Fenton,2001). Thus any generalizations about gland structure are not plausible until a significant number of bats is examined.
MATERIALS AND METHODS
- Top of page
- MATERIALS AND METHODS
- GENERAL DISCUSSION
- LITERATURE CITED
Coronal serial sections of the heads of 20 adult and 5 fetal bat specimens (21 species) were examined (Table 1). This sample included representative species from each of the three major groupings of bats: Pteropodid (Pteropodidae, Rhinopomatidae, Megadermatidae, Rhinolophidae and Hipposideridae: 5 species) and the two derived lineages of Phyllostomatidae/Mystacinaidae (9 species) and Vespertilionidae (7 species; Simmons,2005). The sections were drawn from the vast collection of serially-sectioned heads of bats from the laboratory of one of the authors (KPB). This collection was established over a period of 50 years with specimens donated from all over the world and specimens collected by KPB in the field. Donated specimens were typically preserved in 10% formalin or ethyl alcohol. Whereas specimens collected by KPB were always perfused cardially with either Bouin's fluid, 10% formalin, 4% glutaraldehyde, or other fixatives. The tissues needed were dissected (either in the field and/or in the laboratory) and decalcified using formic acid-sodium citrate solution (for details, see Bhatnagar and Kallen1974a), processed for paraffin embedding, and carried through 10 μm serial sections of the whole head. They were then stained with the Gomori trichrome procedure and other techniques.
|Family||Species||Common name||Fetal Adult|
|Pteropodidae||Rousettus leschenaulti||Rousette fruit bat||Fetal (N = 2)|
|Rhinolophidae||Rhinolophus lepidus||Horseshoe bat||Adult (N = 1)|
|Hipposideridae||Hipposideros lankadiva||Old world leaf-nosed bat||Adult (N = 1)|
|Megadermatidae||Megaderma lyra||Asian false vampire bat||Adult (N = 1)|
|Rhinopomatidae||Rhinopoma microphyllum||Mouse-tailed or long-tailed bat||Adult (N = 1)|
|Mystacinidae||Mystacina tuberculata||New Zealand short-tailed bat||Adult (N = 1)|
|Phyllostomidae||Desmodus rotundus||Common vampire bat||Adult (N = 1)|
|Desmodontinae||Diaemus youngii||White-winged vampire bat||Adult (N = 1)|
|Diphylla ecaudata||hairy-legged vampire bat||Fetal (N = 1)|
|Brachyphyllinae||Brachyphylla cavernarum||Antillean fruit-eating bat||Fetal (N= 1)|
|Glossophaginae||Anoura geoffroyi||Geoffroy's long-nosed bat||Adult (N = 1) and fetus (N = 1)|
|Anoura cultrata||Handley's tailless bat||Adult (N = 1)|
|Phyllostominae||Macrotus waterhousii||Big-eared bat||Adult (N = 2)|
|Stenodermatinae||Artibeus jamaicensis||Neotropical fruit bat||Adult (N = 1)|
|Vespertilioninae||Eptesicus fuscus||House bat||Adult (N = 2)|
|Pipistrellus subflavus||Pipistrelle||Adult (N = 1)|
|Antrozoinae||Antrozous pallidus||Pallid bat||Adult (N= 1)|
|Myotinae||Myotis lucifugus||Little brown bat||Adult (N = 1)|
|Miniopterinae||Miniopterus australis||little long-fingered bat||Adult (N = 1)|
|Miniopterus magnater||Western bent-winged bat||Adult (N =1)|
|Miniopterus schreibersi||Schreibers's long-fingered bat||Adult (N = 1)|
- Top of page
- MATERIALS AND METHODS
- GENERAL DISCUSSION
- LITERATURE CITED
Facial glands, in close proximity to the orbital region were examined. The skin in this region contained varying levels of development of both apocrine sweat and sebaceous glands. Both types are associated with the hair follicles. There was no evidence of eccrine sweat glands on the face. There were five different conditions observed in the relative development of these cutaneous glands (see Table 2 for summary). (1) Hipposideros lankadiva (Fig. 2A) represents the unmodified condition, in that the sebaceous glands are simple branched acinar glands, and the apocrine sweat glands are coiled tubular glands, the endpieces of which pass between the sebaceous glands. These endpieces lie perpendicular to the bases of the sebaceous glands and form a glandular layer that is thinner than that of the sebaceous glands. This is the same condition seen in the skin on the head, and thus is referred to as unmodified. (2) Slightly elongate sweat glands were observed in the nasal, suboccular and postoccular skin of Rhinolophus lepidus (Fig. 2B). In this case, the sweat glands form identifiable lobules which are clearly separated by connective tissue. The apocrine sweat gland layer is thicker than that of the sebaceous gland layer. (3) Still larger apocrine sweat glands are found in the nasal, suboccular and postoccular skin of both Rhinopoma microphyllum and Artibeus jamaicensis (Fig. 2C). In this case, the sweat glands form identifiable lobules which are clearly separated by connective tissue. In this case, the apocrine sweat gland layer is much thicker than that observed in Rhinolophus lepidus.
|Rousettus leschenaulti||? (fetus)||? fetus||+ (fetus)|
|Rhinolophus lepidus||ESW||a: U + L||U|
|Hipposideros lankadiva||N||a: U + L||F|
|Megaderma lyra||N||b: L||LF|
|Rhinopoma microphyllum||LSW||b: U + L||T + F|
|Mystacina tuberculata||N||d: U + L||T + F|
|Desmodus rotundus||LSW||b: U + L||T + F|
|Diaemus youngii||N||c: U + L||T + F|
|Diphylla ecaudata||? (fetus)||b: U||T + F|
|Brachyphylla cavernarum||? (fetus)||? fetus||+ (fetus)|
|Anoura geoffroyi||N||d: U + L||SO|
|Macrotus waterhousii||N||c: U + L||F|
|Artibeus jamaicensis||LSW||d: U + L||T + F|
|Eptesicus fuscus||CSB||b: U + L||T + F|
|Antrozous pallidus||CSB||b: U + L||–s|
|Myotis lucifugus||CSB||b: U + L||F|
|Miniopterus (all 3 spp.)||LSW + LSB||b: U + L||SO + T|
The remaining two conditions are restricted to the vespertilionids and involved the expansion of the sebaceous glands. (4) This was observed in the superior nasal regions of Eptesicus fuscus, Antrozous pallidus and Myotis lucifugus (Fig. 3A) Sebaceous glands are arranged in clusters (or nests), whereby several cells open into a larger central lumen. These glandular clusters then opened via a relatively short duct onto the surface of the skin. These sebaceous glands were not associated with hair follicles. A relatively thin layer of apocrine sweat glands, associated with hair follicles, is found deep to these sebaceous clusters. (5) All three species of Miniopterus, however, exhibit the expansion of both the sebaceous and apocrine sweat glandular tissue. Enlarged, non-clustered sebaceous glands, each with multiple branches (which open onto a hair follicle) lie superficial to the lobules of apocrine sweat glands spread throughout the skin. This occurs specifically in the nasal and perioccular regions. There is also a large suborbital crevasse, lined with these glands (Fig. 3B).
Eyelid glands: Meibomian glands.
The Meibomian glands are the glands of the upper and lower eyelids. They are all sebaceous. However, the bats examined exhibit considerable variation with regards to the relative development of these glands. No Meibomian glands were observed in the eyelids of any fetal specimens. At no stage were there more than four Meibomian glands opening onto the either eyelid. The simplest and smallest Meibomian glands were the same sizes as, and, essentially continuous with the sebaceous glands on the outer part of the eyelid. This pattern is only found in Rhinolophus lepidus and Hipposideros lankadiva (Fig. 4A). Slightly larger specialized sebaceous glands occurred on the inner aspect of the eyelid in several other species, including Megaderma lyra, Rhinopoma microphyllum, Desmodus rotundus and in all vespertilionids (Fig. 4B). A single sebaceous cluster with a single duct is observed in Macrotus waterhousii and Diaemus youngii (Fig. 4C). Finally, a series of sebaceous clusters (3-4) with only 1 duct is observed in Mystacina tuberculata (Fig. 4D), Anoura geoffroyi and Artibeus jamaicensis (Fig. 4E).
Posterior orbital glands: Lacrimal gland.
With the exception of Antrozous pallidus, all bats examined (both adult and fetal) possessed a lacrimal gland. The adult extent and thus position of the lacrimal gland could not be determined in the two taxa of which only fetal specimens were available (Rousettus leschenaulti and Brachyphylla cavernarum). The relative position of the gland with respect to the eyeball varied among species. Though it resides superficial to the eyeball, in the posterior aspect of the orbital region of most bats (with the exception of Anoura, in whom the lacrimal gland is a supraorbital structure and does not seem to be associated with the palpebrae), its association with the palpebra shows some variation. It is found in the upper palpebra of Rhinolophus lepidus (Fig. 5A) and in the fused posterior palpebral region of Hipposideros lankadiva, Macrotus waterhousii and Myotis lucifugus (Fig. 5B). Megaderma lyra has an enlarged lower lid, into which the lacrimal gland extends (as it also protrudes into the fused palpebral region: Fig. 5C). In the remaining bats, the lacrimal gland has a small connection to the palpebral region (Fig. 5D). This is connected by a few small ducts to a large temporal glandular mass, which consists of several lobules. Miniopterus has both a supraorbital portion and a large temporal region. In many cases, lymphatic tissue is associated with the lacrimal gland.
Anterior orbital glands: Harderian and caruncular sebaceous glands.
Several species of bats possess a fat body deep to the eyeball (Fig. 6A). In several specimens, there is a lymphatic aggregation in the orbit anterior to the eyeball. There was little evidence of extra vascularization. The Harderian glands are tubuloacinar glands, usually located in the anterior portion of the orbit, but which may also have lobules penetrating deep into the orbital region. There are also a series of sebaceous glands, simple branched acinar, that reside nearby, on the caruncle. Harderian glands were observed in five species, possibly adding the two species with only fetal specimens examined (Rousettus leschenaulti and Brachyphylla cavernarum). In fetal Rousettus, the Harderian gland appears to be a single tubular structure, extending into the medial orbital region. In fetal Brachyphylla, identification of the Harderian gland was not as clear. Two small puncta/cords occur at the base of the nictitating membrane, but it is uncertain whether they are incipient Harderian or caruncular sebaceous glands at this stage. The Harderian glands of both Artibeus jamaicensis (Fig. 6B) and Desmodus rotundus (Fig. 6C) are relatively small structures confined to the caruncular region. However, in all three species of Miniopterus (Fig. 6D) the Harderian gland is a large, orbital structure, surrounded by periorbital fat. Caruncular sebaceous glands are found in Artibeus jamaicensis (Fig. 6B) Eptesicus fuscus (Fig. 7A), Diaemus youngii (Fig. 7B), and Hipposideros lankadiva (Fig. 4A). Finally, though Anoura has neither a caruncular sebaceous nor a Harderian gland, it does possess a small group of enlarged sebaceous glands (3-4) in a preorbital indentation (Fig. 7C).
Nasolacrimal duct and Vomeronasal organ.
Nasolacrimal ducts spanning the orbital and nasal regions are found in varying length in most bat species examined. The NLD is absent in several members of the Mystacinidae/Phyllostomidae lineage only (Mystacina tuberculata, Desmodus rotundus, Diaemus youngii, Anoura geoffroyi and Macrotus waterhousii). A similar pattern is not observed with the VNO. The VNO is present in Miniopterus and several scattered species of the Phyllostomidae lineage (Desmodus rotundus, Diaemus youngii, Diphylla ecaudata, Anoura geoffroyi, Macrotus waterhousii and Artibeus jamaicensis). Either rudimentary or no VNO is observed in the remaining species. See Tables 2 and 3 for summary of results.
|Miniopterus (all 3 spp.)||+||2||+|
- Top of page
- MATERIALS AND METHODS
- GENERAL DISCUSSION
- LITERATURE CITED
The overriding conclusion that can be drawn from this study is that in terms of the development and distribution of orbital and facial glands, bats show much variation. This is consistent with the level of variation in morphology, ecology and social behavior observed within Chiroptera (Fenton,2001). It is this high level of morphological variation, in addition to conflicting molecular studies that had led to the progressive re-evaluation of bat systematics (Simmons,2005). According to recent analyses (Simmons,2005; MacDonald,2006), the bats examined in this study fall into three main groups (see Fig. 8). The Pteropodids includes Pteropodidae, Rhinolaphidae, Hipposideridae, Megadermatidae and Rhinopomatidae, as comparatively basal taxa. The other two groups consist of the derived bats in the Vespertilionidae and Phyllostomidae/Mystacinidae lineages.
In comparison to that of the orbital glands, there is a more robust literature regarding the facial glands of bats. Bats exhibit much variation in facial structure and various protruberances (Fenton,2001). All such protruberances are more or less glandular (Dalquest and Werner,1954) and are thought to serve primarily in scent marking (Haffner,2000; Caspers et al.,2009). The facial glands in these regions are modified cutaneous glands, namely apocrine sweat and sebaceous glands. However, there appears to be some variation in both the relative development and distribution of these glands among bats.
The results of this study indicate that in the Phyllostomidae, Mystacinidae as well as in the pteropodid group, the only facial gland modification involves an elongation of the apocrine sweat glands. The pararhinal enlarged apocrine sweat glands of Rhinolophus lepidus are an order of magnitude smaller than the apocrine sweat glands (arranged in lobules) observed in 2 species of Rhinopoma (Madkour,1961; Kulzer et al.,1985), Artibeus jamaicensis, Desmodus rotundus and Miniopterus. Though Dalquest and Werner (1954) found no glands in the pararhinal area of Desmodus rotundus, this study found that the pararhinal glands were normally developed. Thus, enlarged apocrine sweat glands are found in scattered species in each of the three main bat lineages. In all remaining bats examined in this study, there appears to be no expansion of the facial apocrine sweat glands.
In contrast, clustered sebaceous glands appear to be largely a vespertilionid feature (see Haffner,1995 for other references), although this study found differences in the level of development among the genera examined. With the exception of Miniopterus, the sebaceous glands of the other vespertilionids form large sebaceous clusters, which consist of 1-4 large lumina surrounded by sebaceous glands. This is an atypical arrangement of sebaceous tissue in mammals. Dalquest and Werner (1954) described such large sebaceous nests (clusters) in the Natalidae (related to the Vespertilionidae) and also in the Emballonuridae, which are currently thought to be a sister taxon to Phyllostomidae (Simmons,1998). However, these glands are reportedly absent, or present as small clusters in the Molossidae (Dalquest and Werner,1954), another lineage closely related to the Vespertilionidae (MacDonald,2006). Haffner (1995) suggested that the location and structure of these glands on the facial protuberances may be ideal for distributing secretions over the body with the head, since bat arms are modified for flight. Thus, within bats' sebaceous glands range from simple glands supporting hair follicles (Rhinolphus lepidus) to the highly specialized scent glands of Myotis (Haffner,2000).
Miniopterus is not only an extreme example of facial gland enlargement, but it also appears to be quite different to the condition seen in other vespertilionids. It is the only genus in this study to possess both enlarged apocrine sweat and sebaceous glands. These sebaceous glands are arranged in a greatly expanded manner, not in the clusters seen in other vespertilionid bats. The sebaceous glands are arranged around a follicle (not a large central lumen, as in other vespertilionids) and are found scattered throughout the skin (both above and below the orbital region). A similar situation occurs in shrews (Mary and Balakrishnan,1991), in which such an expanded nasal glandular region is thought to function in scent marking.
Additionally, Miniopterus also has a suborbital crevasse, which increases the surface area of the skin, thereby increasing number of glands in that region. Though this crevasse has not been previously described in bats, a similar structure has been described in some ungulate mammals, which have a pre-orbital sac, lined by modified skin (like that of Miniopterus) whose integumentary structures have undergone varying levels of development (Schaffer,1940). In the Chinese muntjac (Muntiacus reevesi, Cervidae), the preobital fossa is lined by an epithelium with enlarged apocrine sweat (arranged in lobules) and sebaceous glands (Rehorek et al.,2005b) not unlike those of Miniopterus. Cervus eldi thamin (Cervidae) uses its preorbital gland in scent marking (Müller-Schwarze,1975); perhaps Miniopterus does something similar. Based on the structural similarity, it would be worthwhile to investigate whether Miniopterus has similar marking behaviors.
Lacrimal and Meibomian Glands
Most of the bats examined (except Antrozous pallidus) are typical mammals in that they possess both lacrimal and Meibomian glands. There appears to be no discernible phylogenetic pattern in the relative development of the lacrimal gland among bats as each of the three groups includes species with both very large and smaller lacrimal glands. Furthermore, there is interspecific variation within Hipposideros. Hipposideros speoris possesses a lacrimal gland with a large exorbital region (Korad and Joshi,1992), whereas Hipposideros lankadiva possesses only a lacrimal gland restricted to the eyelid (palpebral lacrimal gland). Hipposideros is a very specious genus of bats, which in modern systemic analyses is often embedded within Rhinolophidae, another specious genus of bats (Nowak,1998). Thus, based upon the level of variation in lacrimal gland size between bat families, variation within a family is not unexpected.
Apart from providing fluid for lubrication, the bat lacrimal gland is also a part of the eye-associated lymphatic tissue. The presence of lymphatic tissue in the orbital region has been described in several amniote tetrapods (Aitken and Survashe,1977; Montgomery and Maslin,1992; Pinard et al.,2003; Rehorek et al.,2005a,2006). As in several other tetrapods the main site for lymphatic tissue is the Harderian gland (Aitken and Survashe,1977; Montgomery and Maslin,1992; Rehorek et al.,2005a,2006), the absence of the Harderian gland in bats may have resulted in a shift of the immunogenic properties towards the conjunctiva and lacrimal glands. Humans also lack a Harderian gland, and, like bats, the lymphatic tissue is found spread out in the conjunctiva and the lacrimal gland (Gillett et al.,1980; Knop and Knop,2000).
Most bats examined possess Meibomian glands. Exceptions are Rousettus leschenaulti and Brachyphylla cavernarum, but because only fetal specimens of these species were examined, the presence of Meibomian glands in adults cannot be ruled out. For the other bats, although there is some variation in relative development of these glands, some generalizations can nevertheless be made. Firstly, the structure of the Meibomian glands in five species (all within the Mystacinidae/Phyllostomidae lineage) differed from that of other mammals, including primates (Montagna and Machida,1966; Gartner and Hiatt,2007), lemmings (Rodentia: Dearden,1959) and both possums and bandicoots (Marsupiala: Green,1963). These bat Meibomian glands comprise of one to four sebaceous clusters with a single excretory pore per eyelid, whereas in the aforementioned mammals, the Meibomian glands are a series of small sebaceous glands. Whether the clustered Meibomian glands observed in these five species of bat produce more sebum than the rows of Meibomian glands observed in other mammals remains to be determined.
Secondly, in the Pteropodid group, as well as in Desmodus rotundus and the Vespertilionidae, it appears that the Meibomian glands are either normal sized (simple branched acinar glands) or slightly enlarged sebaceous glands. The single gland units observed in these bats are morphologically similar to those single gland units described in primates (Miraglia and Gomes,1969; Stephens et al.,1989) and shrews (Mary and Balakrishnan,1991).
Thirdly, the divergence of Desmodus rotundus (with small Meibomian glands) and Diaemus youngii (with clustered Meibomian glands) may be interpreted as either glandular plasticity or bat variation at the intergeneric level. Similar variation was also noted in the precise structure of the Meibomian glands of lemmings (Dearden,1959).
Harderian and Caruncular Sebaceous Glands
There are two identifiably different glands in the anterior part of the orbit in some bat species. The caruncular sebaceous gland is a simple branched acinar gland, associated with a hair follicle in the region of the caruncle, which used a holocrine secretory mechanism. Thus it is termed the caruncular sebaceous gland. The distribution of this gland among bats follows no obvious phylogenetic pattern. It is present in only a few species, once again from each of the three groups of bats: Hipposideros lankadiva (allied with the pteropodid bats), Diaemus youngii (in the more derived group of phyllostomid and their near relatives) and Eptesicus (vespertilionid).
In contrast, the Harderian gland is a tubuloacinar gland using a merocrine secretory mechanism (Payne,1994) of variable size but larger than that of the sebaceous glands, and is usually found deeper in the orbit. This distinction is clearly seen in Artibeus jamaicensis (Fig. 6B), which is thus far the only species in which both glands are present. As the Harderian gland is present in most terrestrial vertebrates, and thus a primitive characteristic for amniotes (see Payne,1994 for review), the absence of this gland in any amniote would be a derived characteristic. However, the distribution of this gland among bats does not neatly follow the current view of phylogeny (see Simmons,2005 for bat phylogeny). It is present, and well developed, in members of two very different lineages, the basal Pteropodidae (Fruit bats: Rousettus leschenaulti) and the more derived vespertilionids (Miniopterus spp.). In contrast it is rudimentary in two more distantly related Phyllostomids (Desmodus rotundus and Artibeus jamaicensis). However, what is most striking about this distribution is that none of the closest relatives of either Miniopterus (including other Vespertilionids such as Antrozous pallidus, Myotis lucifugus and Eptesicus fuscus) or Desmodusrotundus (including Diaemus youngii or any of the other Phyllostomids such as Anouraspp. and Macrotus waterhousii) possess a Harderian gland. This gland is also absent among bats allied with the Pteropodidae (e.g.: Rhinopoma microphyllum, Megaderma lyra, Rhinolophuslepidus and Hipposideros lankadiva).
These observations indicate that Paule's (1957) conclusion that bats have no Harderian glands (based on a single vespertilionid Myotis and a single Phyllostomid Desmodus rotundus) is incorrect on at least two levels. Firstly, based upon the aforementioned variation in bat morphology, generalizations based on two specimens (Paule,1957) will not give accurate results. Secondly, the contradiction between the observations of Paule (1957) and this study, regarding the presence of a Harderian gland in Desmodus rotundus, may be due to sampling technique. Although the precise technique used by Paule (1957) is not known, it has been shown that serial sections are the best way to determine the presence of a Harderian gland, especially if it is small or rudimentary (Rehorek and Smith,2006). There is a further complication within the Desmodontinae, one of which (Desmodus rotundus) possesses a Harderian gland whereas the others possess either a caruncular sebaceous gland (Diaemus youngii) or nothing at all (Diphylla ecaudata, though our specimen was a fetus, perhaps it had as yet to develop).
Generalizations can be made about the nature of the secretant produced by the caruncular sebaceous and Harderian glands. The secretant of the caruncular sebaceous glands usually consists of sebum and is an oily mixture of various lipids and cellular debris. The usual role of sebum lies in maintaining skin and hair flexibility (Gartner and Hiatt,2007). Sebaceous glands may also play a role in scent marking and grooming (Haffner,2000). However, the secretory nature of the Harderian gland is more difficult to determine. The secretory nature of the bat Harderian gland cannot be determined without further histochemical analysis. Numerous functions have been ascribed to the mammalian Harderian gland including grooming and production of melatonin (see Payne,1994 for review).
- Top of page
- MATERIALS AND METHODS
- GENERAL DISCUSSION
- LITERATURE CITED
The relative development of the orbitofacial glands of bats appears to show little correlation with phylogeny. However, a correlation is apparent between the presence of at least one enlarged potentially scent-producing gland (facial and/or Harderian/caruncular sebaceous) and the level of social organization in the specific bat species examined (see Table 4). Bats exhibit many different types of social arrangements, from solitary to short-term aggregations to long-term aggregations leading to the possible formation of a “society” (Fenton,2001). Both Rhinopoma (Sharifi and Hemmati,2002) and Rhinolophus lepidus possess expanded sweat glands and they also exhibit sexual segregation (Nowak,1998; Sedgeley,2003). In contrast, all vespertilionids, which possess enlarged sebaceous glands with multiple lobules, lobulated sweat glands and only moderately developed Meibomian glands (Harrison and Davies,1949; Dalquest and Werner,1954; Haffner,1995,2000; this study) are all highly gregarious and form nursing and or maternal/birthing colonies (Thomas et al.,1979; Nowak,1998; Whitaker,1998). The more complicated the form of social arrangement, the more likely that the animals have developed suitable communication mechanisms.
|Species||Scent gland||HG||Sociality||Relative olfactory bulb size|
|Rousettus leschenaulti||(fetus)||?HG||Loose crowding (Nowak,1998)||42.8|
|Rhinolophus lepidus||FG||MR (Nowak,1998)||28.5|
|Hipposideros lankadiva||CG||No SS (Sapkal and Bhandarkar,1984)||–|
|Megaderma lyra||MG||MR (Nowak,1998)||30.7|
|Rhinopoma microphyllum||FG||MR (Sharifi and Hemmati,2002)||37.5|
|Mystacina tuberculata||MG||SS (Sedgely,2003)||–|
|Desmodus rotundus||FG||HG||SO (Nowak,1998)||45.5|
|Diaemus youngii||CG, MG||SO (Schutt et al,1999)||–|
|Anoura geoffroyi||MG, PI||SS (Nowak,1998)||–|
|Macrotus waterhousii||MG||MR (Nowak,1998)||40.0|
|Artibeus jamaicensis||CG, FG, MG||HG||SO (Kunz et al,1983; Ortega and Arita,1999)||50.0|
|Eptesicus fuscus||CG, FG||MR + NC (Nowak,1998)||–|
|Antrozous pallidus||FG||MR + NC (Nowak,1998)||35.3|
|Myotis lucifugus||FG||MR + NC (Nowak,1998)||42.8|
|Miniopterus (all 3 spp.)||FG||HG||MR + NC (Nowak,1998)||–|
Bats use many channels for communication, but chemical and vocal communications are the main ones. In addition, the more complex the behaviour is (e.g., sex attraction is relatively simple whereas recognition signals are more complex) the more complex the chemical compound that is produced to facilitate it (Alberts,1992). Scent-producing glands are usually the source of such secretions. Thus, the morphological results need to be compared to known observations of the chemical senses. The two best described are the vomeronasal and the olfactory senses.
Role of Glands As Cues for the Vomeronasal System
It has been proposed (Hillenius and Rehorek,2005) that primitively, the Harderian gland secretions may have led into the VNO and served some function in the vomeronsal sense. This suggestion was based upon the connection between the Harderian gland and the VNO via the NLD observed in many amphibians and reptiles. However, in mammals, the VNO is rarely closely associated with the NLD (Hillenius and Rehorek,2005; Rossie and Smith,2007). This may be due to the reduction or loss of the septomaxillary bone, which was associated with the rostral terminus of the NLD in primitive tetrapods (Hillenius,2000). In bats, however, there is much variation in the presence and relative development of both the NLD and the VNO (see Table 3; Göbbel,2002). This, once again, however, appears to have little clear congruence with bat phylogeny (see Table 3). The clearest pattern is observed in the pteropodid group, in whom all the species examined had a shortened NLD. Members of the Pteropodidae itself lack a VNO altogether (Bhatnagar et al.,1996) and the VNO is rudimentary in most of the remaining taxa allied with the pteropodids (Cooper and Bhatnagar,1976). Thus, although at least one member of this group, Rousettus leschenaulti, retains a Harderian gland, its orbital secretions cannot play a role in the VNO function, since the VNO is absent. This condition parallels that of archosaurs, in which a well-developed Harderian gland and NLD, but no VNO, have been described (Rehorek et al.,2005a). In that case, it has been suggested that the Harderian gland in these animals may play a role in the mucosal immune system, as suggested by the large lymphatic aggregations present in the stroma (Rehorek et al.,2005a). The Harderian gland has apparently been lost in other species in the pteropodid group. The loss of the Harderian gland in these bats may be associated with the reduction of the VNO, but further investigation is needed to confirm this possibility.
The pattern is less clear among the remaining bats. In the Mystacinidae and Phyllostomidae, which appear to share a common ancestor, the NLD is either lacking or rudimentary. The VNO, on the other hand, is usually well developed (it is rudimentary in Brachyphylla). In this group, several unrelated species possessed Harderian glands (Desmodus rotundus, Artibeusjamaicensis and possibly Brachyphylla cavernosum). Once again, this condition is not unique. In turtles, the Harderian gland has also been disconnected from the VNO through the loss of the NLD (Hillenius and Rehorek,2005). In most turtles the Harderian gland is thought to function in orbital lubrication, but it has been suggested that to play a role in osmoregulation in several aquatic turtles (Cowan,1971). It is not known whether the Harderian glands have an osmoregulatory function similar to those of turtles. In any case, the Harderian gland, small as it is in these three species of bats, could play a functional role in the orbital region.
With the exception of Miniopterus, the vespertilionid bats possess no VNO and have a variably developed NLD. The NLD opens either into the floor of the nostril (Eptesicus fuscus, Antrozous pallidus, Myotis lucifugus) or near the nasopalatine duct/VNO (Miniopterus). In either case, secretions from the orbital region pass into the nasal cavity. The condition in Miniopterus is reminiscent of the primitive tetrapod condition (wherein the NLD open in the vicinity or the VNO, Hillenius and Rehorek,2005), but that of the other three vespertilionids is reminiscent of the typical mammalian condition. This is exemplified by rodents, including the mongolian gerbil, in which the secretions for the orbital region pass through the NLD and exit at the nares, only to be smeared over the body (Thiessen,1992). However, unlike rodents, these vespertilionid bats lack a Harderian gland.
Miniopterus deserves special attention. It is the only bat in this study to possess a Harderian gland, a VNO and a NLD that opens in the vicinity of the VNO, and is reminiscent of the primitive tetrapod condition (Hillenius and Rehorek,2005). However, Miniopterinae (Miniopterus) are currently not thought to be the most primitive subfamily of Vespertilionidae. It is currently placed between the Myotinae (Myotis)/ Vespertilioninae (Eptesicus) lineage and the Antrozoinae (Antrozous) lineage (Simmons,1998). However, all three of these species (Myotis, Eptesicus and Antrozous) lack both a VNO and a Harderian gland (although they possess a full length NLD), and thus appear to be more derived than Miniopterus. These anatomical observations are difficult to reconcile with the phylogenetic position of Miniopterus in the Vespertilionidae and thus needs to be revisitied. With the exception of Miniopterus, it may be concluded that there is no consistent pattern between the presence of a Harderian gland and the relative development of the VNO and NLD in bats. Instead, there is a lot more variation in bat HG-NLD-VNO morphology than in most other described vertebrates.
The condition in Antrozous pallidus is unusual. This species lacks a Harderian gland, a lacrimal gland, and a VNO, although it retains a full-length nasolacrimal duct. If the primary role of the nasolacrimal duct is to drain orbital fluid into the nose, then the role of this structure in Antrozous pallidus needs to be re-examined. The presence of such a well developed duct in the absence of large glands (except a pair of enlarged tarsal glands) raises questions about the presumed drainage role for this structure and the source of orbital lubricants needs to be determined for this taxon. Lymphatic tissue is spread throughout the conjunctiva.
Thus, in conclusion, the results of this study imply that the relative development of the orbitofacial glands of bats is not correlated with either that of the NLD or the VNO. As it has been suggested that the HG-NLD-VNO axis may be the primitive condition (Hillenius and Rehorek,2005), the loss of any of these component may thus be presumed to be indicative of a derived condition. This has been described in turtles (which lack a NLD: Saint Girons,1988), archosaurs (birds and crocodilians: which lack a VNO: Rehorek et al.,2005a) and several primates (which lack a HG and possibly a VNO: Rehorek and Smith,2006). Bats are unique in that they not only are indicative of the derived condition, but also that they exhibit more variation in the HG-NLD-VNO axis than all the other tetrapods combined.
Role of Glands As Cues for the Olfactory System
The size of these potential scent-producing glands and the level of communality can also be correlated to relative development of olfactory system (see Table 4). One indirect measurement of olfactory acuity may be the ratio of olfactory bulb diameter to cerebral hemisphere diameter. Although we acknowledge that ratios may be misleading (Smith and Bhatnagar,2004) other means of assessing relative size (such as calculation of residuals) are impractical due to the small sample size. Based on these ratios, the proportionally largest olfactory bulbs in bats has been recorded in Artibeus jamaicensis (Bhatnagar and Kallen,1974a,b). Not only does this species exhibit more anatomical development of both the olfactory and visual structures (Bhatnagar,1975), but it also possesses lobulated apocrine sweat glands. The ducts of these glands are associated with hair follicles, which is typical for glands that play a role in scent production (Gartner and Hiatt,2007). Enlarged apocrine sweat glands have also been described in lagomorphs (Lyne et al.,1964) and rodents (Rausch and Bridgen,1989) in which they are presumed to play a role in scent marking (objects and individuals). Thus, the presence of lobulated apocrine sweat glands is consistent with the contention that Artibeus jamaicensis uses olfaction to a greater degree than most other bats. The olfactory system in Artibeus jamaicensis may not only function in finding food (frugivorous bats appear to have a greater olfactory acuity than nonfrugivorous bats: Bhatnagar and Kallen,1974a,b), but may also be explained by their level of social organization. These bats form complex social units, namely harems (Kunz et al.,1983; Ortega and Arita,1999) and individual identification is apparently very important. Such information may be passes along chemically using the lobulated apocrine sweat glands.
The second proportionally largest olfactory acuity has been recorded in Desmodus rotundus (Bhatnagar and Kallen,1974b; Bhatnagar,2008). This sanguivorous bat also possesses lobulated apocrine sweat glands. Desmodus rotundus forms some recognizable social units (Nowak,1998). In this case, the relatively well developed olfactory system of these bats may be explained by a combination of social structure and dietary requirements. In Diaemus youngii (also sanguivorous, and a close relative of Desmodus rotundus) there are additionally some recognizable social units, although there is little evidence of enhanced facial glands. Though the relative development of the olfactory system of Diameus youngii is unknown, it does not appear to use chemical signaling during threat behavior, e.g.: the exposure of a pair of large oral glands of the newcomer male and the insertion of the tongue onto these glands by the dominant male (Schutt et al.,1999). Further investigation of the olfactory acuity of Desmodontinae is thus needed.
Though not as large as either Artibeus jamaicensis or Desmodus rotundus in size, the insectivourous vespertilionid bats still have a relatively well developed olfactory system (Bhatnagar and Kallen,1974a,b; Bhatnagar,1975). Though the relative development of the olfactory system in vespertilionids may be correlated to their feeding lifestyle (Bhatnagar and Kallen,1974a,b), it does not seem to explain the level of facial glandular development seen in these bats. At this stage, it become necessary to separate out Miniopterus from the other vespertilionids, as the structure of their facial glands is significantly different from that of the others. Vespertilionids, other than Miniopterus, possess large facial glands, but unlike that of either Artibeus jamaicensis or Desmodus rotundus, they are sebaceous glands, with relatively underdeveloped associated sweat glands. Such a combination of glands was also described in lagomorphs (Mykytowycz,1966). Further chemical analysis of this chemical mixture led Goodrich and Mykytowycz (1972) to conclude that the sebaceous portion of the secretant may function as a fixing medium for the apocrine sweat secretions (which were reported to have a “rabbity” smell). The clustered sebaceous glands may have a similar function in vespertilionid bats: the copious amount of sebum produced by these clustered sebaceous glands may act to keep the secretions of sweat glands on the body or substrate. Since vespertilionids are gregarious and highly social, this mixture of sebaceous and sweat secretions may be smeared upon individuals. This mixture would then function more as a more permanent identifier (with the sebum functioning as glue for the sudoriparous apocrine secretions) than just sweat secretions alone (which are volatile and prone to dissipation when the bat searches for food).
Miniopterus, once again, is an extreme example. Alone among the vespertilionids, this genus has a large Harderian gland as well as a suborbital crevasse lined by lobulated sweat and sebaceous glands. This anatomical arrangement is reminiscent of that in ungulates. In deer, it has been suggested that secretions from the Harderian gland may flow into the preorbital fossa (Rehorek et al.,2005b), which would further enhance the chemical mixture in the sac. It is this solution that is then used for chemical communication. Something similar could be happening in Miniopterus. Whereas all vespertilionids form maternal/birthing or nursing colonies, Miniopterus forms the largest nurseries (Miniopterus nursery colony can contain up to 110,000 juveniles, one female per juvenile, compare to Eptesicus fuscus: 10–14 females, Antrozous pallidus: 12–100 females and Myotis lucifugus: 15–1,110 females: Nowak,1998). The young are deposited in these very large nurseries (under the care of other bats) whilst the mother goes out foraging (Nowak,1998). Thus, an efficient and specific form of recognition would be vital to locate the baby bat. This may explain why Miniopterus have such well developed glands.
Enlarged sweat glands were also observed in Rhinolphus lepidus and lobulated sweat gland in Rhinopoma kinneari. The olfactory system is either less (Rhinolophus) or equally (Rhinopoma) well developed as in vespertilionid bats (Bhatnagar and Kallen,1974a,b). The rabbit chin glands, also lobulated sweat glands (Lynne et al.,1964), lack any actual smell (Goodrich and Mykytowycz,1972). Both these bats (Rhinolophus and Rhinopoma) and the rabbit chin gland possess normally developed sebaceous glands. Thus not all sweat glands may function in scent marking or social communication.
The relative development of facial glands in adult specimens of Rousettus leschenaulti (Pteropodidae) and Brachyphyllacavernarum (Phyllostomidae) remains to be described. The fetal specimens of both species possess either a Harderian gland (Rousettus leschenaulti) or a primordium that may develop into a Harderian gland (Brachyphylla cavernarum). Neither of these species exhibits much in the way of a social organization, though Rousettus does have marked sexual dimorphism (Nowak,1998). Thus, alternate functions for the Harderian gland need to be considered. It is unlikely to function in the vomeronasal sense, since the VNO is either absent (Rousettus) or rudimentary with an incomplete NLD (Brachyphylla cavernarum). In the case of Rousettus leschenaulti, the presence of a well developed NLD, opening into the nasal cavity, is reminiscent of the archosauran condition (Rehorek et al.,2005a), in which, the presence of lymphatic tissue indicates a role in the immune system. A similar function may occur in Rousettus, though further investigation using adult specimens is required.
The condition in Brachyphyllacavernarum depends upon what the primordial bud develops into. If it is a Harderian gland, then it will be the third phyllostomid with a Harderian gland, but the only one without a VNO. Thus, this will mean that there are at least two departures from the phyllostomid condition (VNO with no or rudimentary NLD). On the other hand, if the primordium ends up being a caruncular sebaceous gland (as seen in the Desmodontinae), then Brachyphylla will be a more typical phyllostomid bat with a rudimentary VNO as a stand out feature. Further examination of an adult Brachyphyllacavernarum would thus be more instructive.
The comparative structure of bat facial and orbital glands is highly diverse, and few clear patterns, whether phylogenetic or function, are apparent. What can be unequivocally concluded is that Paule's (1957) assertion that bats have no Harderian glands is incorrect. The function of these glands, however, remains largely unknown, although future examination and correlation with social behavior may prove instructive. The role of the other orbital glands may involve immunological and lubricatory aspects. With respect to the facial glands, the level of development of these glands may be correlated to the relative development of the olfactory system and social structure, though it should be noted that not all glands function in the same manner. Chemical analysis of these glands is needed to further elucidate any potential role that they may have.
- Top of page
- MATERIALS AND METHODS
- GENERAL DISCUSSION
- LITERATURE CITED
The authors thank W. Hillenius for criticism of this article. The specimens used in this study were all either received from colleagues, collected in the wild by KPB, or obtained from museums for a long-term, ongoing, study on the vomeronasal organ of bats. Appropriate acknowledgments have been made to these sources in the publications, some of which are cited in this work. For Mystacina tuberculata, the authors are grateful to Dr. James Dale Smith. The authors acknowledge the generous help of Kamar Karim (Rousettus), the late William A. Wimsatt (Desmodus, Artibeus), David Nellis (Brachyphylla), Paul Heideman (Anoura geoffroyi), John Wible, Carnegie Museum of Natural History (Anouracultrata), and Heinz Stephan (Miniopterus magneter). The serially sectioned heads of over fifty species of bats, collected over some 40 years is now housed at Slippery Rock University under the care of Timothy Smith for use by bat researchers. The preserved specimens (whole, dissections, skeletal preparations) are housed at the Department of Biology, University of Louisville, under the curatorial supervision of Jennifer Jones.
- Top of page
- MATERIALS AND METHODS
- GENERAL DISCUSSION
- LITERATURE CITED
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